Brazilian Journal of Biology http://dx.doi.org/10.1590/1519-6984.172814 ISSN 1519-6984 (Print) Original Article ISSN 1678-4375 (Online)

Understanding mammary activity in red-rumped and implications for management and conservation of this Neotropical game M. D. Singha*, S. Singhb and G. W. Garciaa aDepartment of Food Production, Faculty of Food and Agriculture, The University of the West Indies, St. Augustine, Trinidad and Tobago bBiochemistry Unit, Department of Preclinical Sciences, Faculty of Medical Science, The University of the West Indies, St. Augustine, Trinidad and Tobago *[email protected]

Received: November 29, 2016 – Accepted: March 15, 2017 – Distributed: October 31, 2018 (With 4 figures)

Abstract The red-rumped agouti (Dasyprocta leporina) produces precocial young and is the most hunted and farmed game species in several Neotropical countries. An understanding of the reproductive biology, including the relationship between litter size and teat functionality is crucial for conservation management of this . In precocial mammals, as the red-rumped agouti, maintaining maternal contact to learn foraging patterns may be more important than the energy demands and nutritional constraints during lactation and suckling may not play important roles when compared to altricial mammals. Therefore, in this study we evaluated the relationship between mammary functionality with litter size, litter birth weight, and parturition number in captive red-rumped agouti. Functionality was assessed by manual palpation of teats from un-sedated females (N=43). We compared the average birth weight of all newborns, male newborns and female newborns among with different litter sizes and different parturitions by one way ANOVA’s, while Pearson’s Chi-squared tests were used to detect relationships between teat functionality, litter size, and parturition number. Parturition number had no effect on the mean birth weight of all young F( 0.822, P > 0.05), male young (F0.80, P > 0.05) or female young (F0.66, P > 0.05) in the litters. We found (i) no significant correlations P( > 0.05) between teat functionality and litter size and (ii) no significant correlations (P > 0.05) between teat functionality and parturition number. This suggests that whilst all teat pairs were functional, functionality was a poor indicator of litter size; suggesting that female agouti young may not have a high dependency on maternal nutrition; an possible evolutionary strategy resulting in large wild populations; hence its popularity as a game species. Keywords: animal reproduction, agouti, Dasyprocta leporina, teat functionality, weaning age.

Compreendendo a atividade mamária na cutia e as implicações para o manejo e a conservação desta espécie cinegética Neotropical

Resumo A cutia (Dasyprocta leporina) produz filhotes precoces, e é a espécie cinegética mais caçada e criada em muitos países neotropicais. O entendimento da biologia reprodutiva, incluindo a relação entre o tamanho da ninhada e a funcionalidade das glândulas mamárias é crucial para o manejo conservacionista deste animal. Nos mamíferos precoces, como a cutia, manter o contato materno para a aprendizagem de padrões de forrageamento pode ser mais importante do que a demanda energética e de restrição nutricional durante a lactação, e a amamentação pode não desempenhar um papel importante quando comparado aos mamíferos altriciais. Portanto, neste estudo nós avaliamos a relação entre a funcionalidade mamária com o tamanho da ninhada, peso ao nascer da ninhada, e o número de partos em cutias cativas. A funcionalidade foi avaliada por meio de palpação manual das glândulas mamárias em fêmeas não sedadas (N=43). Nós comparamos a média do peso ao nascer de todos os recém-nascidos, macho e fêmeas recém-nascidos entre cutias com diferentes tamanhos de ninhadas e diferentes parturições, por meio da análise one–way ANOVA unifatorial; enquanto o teste do chi-quadrado de Pearson foi utilizado para detectar as relações entre a funcionalidade da glândula mamária, o tamanho da ninhada e o número de partos. O número de partos teve efeito na média de peso ao nascer dos filhotes F( 0,822, P > 0,05), filhotes machos F( 0,80, P > 0,05) ou filhotes fêmeas F( 0,66, P > 0,05) nas ninhadas. A análise bivariada de Pearson (i) não mostrou correlação (P > 0,05) entre a funcionalidade da glândula mamária e o tamanho da ninhada e (ii) nenhuma correlação significativa P( > 0,05) entre a funcionalidade da glândula mamária e o número de parições. Os resultados sugerem que, embora todos os pares de tetas fossem funcionais, as cutias recém-nascidas

540 540/547 Braz. J. Biol., 2018 , vol. 78, no. 3, pp. 540-547 Mammary functionality in Dasyprocta leporina in captivity podem não depender da nutrição materna para sobreviver; .embora todos os pares de tetas sejam funcionais, as cutias recém nascidas aparentemente não dependem da nutrição materna para sua sobrevivência; esta é, provavelmente, uma estratégia evolutiva que resulta em grandes populações da cutia em vida livre; e que pode explicar sua popularidade como espécie cinegética Palavras-chave: reprodução animal, cutia, Dasyprocta leporina, funcionalidade mamária, idade ao desmame.

1. Introduction (Baas et al., 1976; Deem, 2012). It is a non-seasonal breeder (Baas et al., 1976; Campos et al., 2015; Guimarães et al., 2011; The length of lactation in mammals is influenced by Singh et al., 2014) and under captive conditions, when the quality and quantity of milk produced, body size, and receiving an abundance of food with a high plane of age of the mother (Oftedal, 2000). The mammal’s ability nutrition may produce larger litters (Singh and Garcia, to produce milk is determined by the level of activity and 2015). Agoutis reach puberty at eight months and go number of secreting cells (Hughes, 1950; Kim et al., 1999). through gestation for 104 to 120 days Teat functionality can be measured by the increased (Guimarães et al., 2011; Lopes et al., 2004; Weir, activity of the mammary glands through the ability of 1971) producing litters between one and six young the teat to yield milk (Farmer, 2013; Hughes, 1950). (Brown-Uddenberg et al., 2004; Dollinger et al., 1999; The quality and quantity of milk, however, may change Lopes et al., 2004; Singh and Garcia, 2015). Gestational according species, maternal nutrition, habitat, and water intervals of 115 to 190 days (Korz, 1991; Meritt, 1983; availability (Kim et al., 1999). Each one of these glands Roth-Kolar, 1957) and 219 days (Dubost et al., 2004) is comprised of tubular-alveolar epithelium, mainly have been reported for the agouti. This long interval can composed of epithelial cells where milk is synthesized potentially be manipulated in captivity, especially as agoutis (Hughes, 1950; Robinson et al., 1999) and is then secreted do not exhibit lactational anestrous (Guimarães et al., 2009; into the alveolar lumen through a network of ducts to the Weir, 1971). glandular cistern. In captive breeding programs for conservation Mammary cell activity and milk yield is stimulated and production, the rate of reproduction and offspring by increased milking frequency (Knight and Wilde, 1987; survivability are crucial factors which affect conservation Knight and Wilde, 1993) and suckling from one parturition efforts and farmers’ production and profitability; thus, the to the next (Farmer, 2013). The mammary glands are located parameters which affect these are important. Hence, to in varying positions in the thoracic to inguinal region improve agouti production in captivity the relationship of the body (Gilbert, 1986; Pagels, 2013). The number between mammary functionality and litter size needs to of activated mammae/functional teats may have acted be understood. In mammals that bear precocial young like as a selective constraint in litter size of wild mammals agouti (Smythe, 1978), maintaining maternal contact to (Korhonen, 1992). Thus, teat functionality is an aspect learn foraging patterns may be more important than the that may be considered in domestication of new species energy demands and nutritional constraints during lactation (Deem, 2012). Within these species, the agouti (Dasyprocta (Pond, 1977), suggesting that lactation and suckling may leporina) (Linnaeus, 1758) is highly prized for its meat and not play important roles when compared to altricial . one of the most consumed game species in Neotropical As female agoutis do not experience lactational anestrous countries (Cummins et al., 2015; Robinson and Redford, (Guimarães et al., 2009), we considered that lactation may 1991). Despite the species classification as ‘Least Concern’, not be as important for nutrition and survival of newborn overhunting may compromise its survival (Emmons agouti. Thus, we predict that we will find no relationships and Reid, 2016). To avoid this, some authors suggested between mammary functionality with litter size, litter birth the agouti and other Neotropical species for captive weight, and parturition number. production systems (Nogueira and Nogueira-Filho, 2011; Perez and Ojasti, 1996). In Brazil, there were just 21 legal 2. Materials and Methods agouti farms (Le Pendu et al., 2011), while in Trinidad and Tobago over 400 wildlife farmers rear the agouti in 2.1. Ethical approval captivity (Rackal et al., 2013). Hence the question arises All applicable international, national, and/or institutional on whether this species maintains teat functionality for guidelines for the care and use of animals were followed. extended periods of time, and whether teat functionality is related to litter size, parturition number or litter birth 2.2. Animals and housing weight. This will inform on the need for a weaning period Forty-three pregnant female agoutis, aging between in captive colonies of agouti, influencing gestation interval 2-4 years, were individually housed with their young in and reproductive efficiency and ultimately conservation wire mesh cages (0.6m wide x 0.6m deep x 0.9m high) activities. over a period of 10 months in 2014 at the Agouti Unit, The agouti is a of an average weight of 4.5 kg. Department of Food Production, Faculty of Food and The female agouti has eight mammae, two pairs in the Agriculture, The University of the West Indies, St. Augustine, thoracic region and two pairs in the abdominal region Trinidad and Tobago. Females had a mean (± SD) body

Braz. J. Biol., 2018 , vol. 78, no. 3, pp. 540-547 541/547 541 Singh, M.D., Singh, S. and Garcia, G.W. weight of 4.3 (± 1.2) kg before mating and comprised of were weighed on the day of birth and examined by manual primiparous (N=10) and multiparous females (N=33). palpation to determine sex. The animals were watered and fed ad libitum with diets 2.4. Statistical analyses consisting of Mangifera indica, Musa spp., Curcubita pepo, Anacardium occidentale, Cocos nucifera, Manihot The dependent variable was teat functionality, while esculenta, Ipomea batatas, Leucaena leucocephala, and litter size, litter birth weight, litter sex and parturition Trichanthera gigantea. number were independent variables. The data set was recorded into agoutis with litter sizes ranging from 2.3. Milk and data collection one to two and those with litter sizes greater than two. Milk collection began one day after birth and continued Pearson’s Chi-squared test was used to detect possible three times weekly until weaning at four weeks. Each female associations between teat functionality (at the various agouti was manually restrained and milk collected from pairs), litter size, litter birth weight and parturition number. each teat using a modification of the method described Pearson’s bivariate correlation analysis was used to detect by De Peters and Hovey (2009). Briefly, each teat was significant relationships between teat functionality and litter gently massaged and plucked for milk yield. Based on size/parturition number. One-way Analysis of Variance its location, each pair of agouti teat was identified as the (ANOVA) was used to compare the birth weight of all cranial pair (CrP), abdominal pair 1 (AP1), close to the young, male young and female young among agoutis from head, abdominal pair 2 (AB2), close to the rear and the caudal pair (CaP) (Figure 1). different litter sizes and different parturition numbers. The presence or absence of milk droplets from the The Bonferroni and Least Squares Difference post-hoc functional teats over a four-week period was recorded. tests were used to determine where significantly different A mammary teat pair was considered functional if both means existed. All statistical analyses were performed teats produced milk at the same time or non-functional if using the Statistical Package for Social Sciences (SPSS) it did not produce milk simultaneously. Subsequently, the 20 software for Windows (IBM, NY, USA). longitudinal data for each pair of teat (CrP, AP1, AP2, and CaP) was dichotomized and recoded to reflect functionality 3. Results for an entire 28 day period vs. non-functionality for any part The CrP was functional in 42 (98%) female agoutis thereof. Frequency tables were generated to describe the (Figure 2a), while AP1, AP2, and CaP was functional in data set according to litter size and parturition number and 22 (51%) (Figure 2b), 9 (20%) (Figure 2c) and 19 (44%) also to report the functionality of each teat pair. Newborns (Figure 2d) female agoutis, respectively. Thirty four (79%) of female agoutis had a litters of one or two young and nine (21%) had litters with more than two young (Figure 3). Ten (23%) of the agoutis had one parturition, while 13 (30%) had three, 11 (26%) had 2, eight (19%) had four, and just one (2%) had five parturitions Figure( 4). There were no significant associations between the 2 functionality of teat pairs CrP (χ 1 = 0.27, P > 0.05), 2 2 AP1 (χ 1 = 1.45, P > 0.05), AP2 (χ 1 = 0.01, P > 0.05) or 2 CaP (χ 1 = 0.0003, P > 0.05) and litter size. There were also no significant associations between the functionality of teat 2 2 pairs CrP (χ 4 = 2.98, P > 0.05), AP1 (χ 4 = 2.05, P > 0.05), 2 2 AP2 (χ 4 = 0.44, P > 0.05) or CaP (χ 4 = 3.77, P > 0.05) and parturition number. Pearson’s bivariate analyses revealed (i) no correlations between teat functionality and litter size for CrP (R = -0.20, P > 0.05), AP1 (R = 0.29, P > 0.05), AP2 (R = 0.24, P > 0.05), and CaP (R = 0.28, P > 0.05), and (ii) no correlations between teat functionality and parturition number: CrP (R = -0.07, P > 0.05), AP1(R = -0.20, P >0.05), AP2 (R = -0.02 P > 0.05) and CaP (R = 0.20, P > 0.05). Mean (± SE) birth weight of young in litters with single

births (N=10) was significantly higher (F4.20, P < 0.05) than young from litters of two young (N=24) and three young Figure 1. Diagram of agouti in lateral recumbence showing (N=6) births (Table 1). Mean (± SE) birth weight of male location of the Cranial teat Pair (CrP), Abdominal teat young in litters with single births (N=5) was significantly

Pair 1 (AP1), Abdominal teat Pair 2 (AP2) and Caudal teat higher (F2.29, P < 0.05) than male young from a litter of Pair (CaP). two young (N=24) births (Table 1). Parturition number had

542 542/547 Braz. J. Biol., 2018 , vol. 78, no. 3, pp. 540-547 Mammary functionality in Dasyprocta leporina in captivity

Figure 2. Percentages of functional teat pairs in female agoutis (N=43). (a) Cranial teat Pair (CrP); (b) Abdominal teat Pair 1 (AP1); (c) Abdominal teat Pair 2 (AP2), and (d) Caudal teat Pair (CaP).

Braz. J. Biol., 2018 , vol. 78, no. 3, pp. 540-547 543/547 543 Singh, M.D., Singh, S. and Garcia, G.W. no significant effect on the mean birth weight of all young as well as in marsupials (5-12 nipples) (Hayssen, 1993;

(F0.822, P > 0.05), male young (F0.80, P > 0.05) or female Senger, 2013). young (F0.66, P > 0.05) in the litters (Table 2). As we expected, due to the precocial characteristic of agouti young (Sikes and Ylonen, 1998; Smythe, 1978), 4. Discussion the teat functionality was not related to litter size, litter birth weight, and parturition number in female agouti. In In the agouti, the cranial pair was functional in a great majority of the females, making it the most functional pair. mammals that bear precocial young, as agoutis (Smythe, Teat functionality varies, and mammals that are primarily 1978), young can rapidly obtain relatively large amounts monotocous like cattle have four functional teats, whereas of milk with each compression of the teat, as these species humans, primates, elephants, sheep and goats have two represent prey to large predators, hence the ability to feed (Anderson et al., 1982). In polytocous species, like the rapidly and flee quickly is highly adaptive survival traits agouti, teat functionality has never been investigated, (Pagels, 2013). It has been suggested that with increasing however, the number of active nipples can vary with litter litter size, there is an associated increase on energetic size, and may be considered inversely proportional as requirements and this may limit litter size due to energy litter size can exceed available nipples as seen in guinea requirements of the mother for lactation and maintenance pigs (2 nipples), rats, dogs, cats and pigs (7-12 nipples) (Sikes and Ylonen, 1998). Precocial young, as agouti,

Figure 3. Litter sizes among female agoutis (N=43). Figure 4. Parturition number among female agoutis (N=43).

Table 1. Mean (± SE) birth weight (g) of all young, male young and female young in different litter sizes. Litter Size Variable 1 2 3 4 310a ± 17 255b ± 8 249b ± 17 275.78ab ± 24 All n=10 n=24 n=6 n=3 321a ± 33 259a ± 12 234b ± 20 245b ± 12 Male n=5 n=24 n=6 n=3 300 ± 9 251 ± 11 264 ± 24 304 ± 34 Female n=5 n=24 n=6 n=3 abMeans in the same row followed by different superscript letters differed by the t testP ( < 0.05).

Table 2. Mean (± SE) birth weight (g) of all young, male young and female young in agoutis with different parturition numbers. Parturition Number Variable 1 2 3 4 288 ± 17 270 ± 18 260 ± 12 256 ± 10 All n=10 n=11 n=13 n=9 281 ± 20 249 ± 31 253 ± 16 264 ± 14 Male n=10 n=8 n=11 n=9 289 ± 23 263 ± 14 255 ± 18 248 ± 15 Female n=9 n=10 n=12 n=7

544 544/547 Braz. J. Biol., 2018 , vol. 78, no. 3, pp. 540-547 Mammary functionality in Dasyprocta leporina in captivity however, are born with eyes open, well furred and little and Peres, 2005; Nasi et al., 2011; Robinson and Redford, dependence on maternal nutrition (Sikes and Ylonen, 1991) in hunted areas, making the agouti one of the most 1998; Smythe, 1978). In such precocial mammal species, common forest mammal. This species reproduces quickly maintaining maternal contact to learn foraging patterns may (Dubost et al., 2004; Ojasti, 2000; Roth-Kolar, 1957; be more important than the energy demands and nutritional Weir, 1971) and hence has a better chance of surviving constraints during lactation (Pond, 1977), suggesting hunting pressure. The tolerance to harvesting may be that lactation and suckling may not play important roles related to the biology of the agouti; the reproduction when compared to altricial animals. In contrast, species potential and survivablility of the animal which influences that bear altricial young, like the opossum (Didelphis the recruitment of agoutis into the population (Robinson marsupialis) with litters ranging from 4 to 25 young and Redford, 1994). The higher the number of animals born in the embryologic state, there is a strong positive recruited into the population, the greater numbers are correlation between litter size and teat functionality and available to be harvested. This evolutionary survival number, since neonates which do not attach to a nipple strategy would explain the popularity of the agouti as a perish (Feldhammer et al., 2003). game species and also make it an ideal species for captive Parturition number (one to four) had no effect on production systems. neither individual nor total litter birth weight in captive The teat functionality, as we expected, due to the agoutis. This is in contrast with reports on captive capybaras precocial characteristics of the species, was not correlated (Hydrochoerus hydrochaeris) as litter size was apparently to litter size or birth weight in captive agouti. This suggests affected by maternal age, with a sharp decrease occurring that newborn agouti may not be dependent on suckling by the fourth birth (Nogueira-Filho and Nogueira, 2013). for nutrition, as is seen in other precocial mammals, These differences may be due to the duration of this study and can be used to guide management of captive agouti as data only up to the fourth parturition was collected, production systems for conservation and production while in the capybara study, the authors analyzed up to as it may be possible to wean neonatal agoutis almost the eighth parturition. Usually, life history variables like immediately, returning the mother to breeding thereby parturition number has often shown a negative relationship reducing the parturition interval, increasing productivity between litter size and offspring weight, with multiparous in captivity. Our data also may help to explain the large females producing increasingly larger litters (Sikes and populations of wild agouti, which persist even in heavily Ylonen, 1998). This can be explained by body mass. As the hunted Neotropical areas, as young, apparently, have little animal ages, body mass increases, thereby improving the dependence on maternal milk. physiological adaptations for larger litters (Westlin and Gustafsson, 1983). Thus, further study with older agoutis Acknowledgements may confirm our results. In this experiment, birth weights were higher for male We wish to express gratitude to Mr. Adnan Maharaj and and female newborn agoutis (251g, 310g), than reports Mr. Birendra Dookie for their assistance in animal restraint by Lopes et al. (2004), who recorded 149g for both sexes and sample collection at the Agouti Unit, as well as to in black-rumped agouti, 172g from D. prymnolopha and Prof. Sérgio Nogueira-Filho for his invaluable comments D. aguti and 148g and 146g. These were similar to weights on the paper. reported by Meritt (1983) who stated a value of 258g (range 210-308g) from male newborn agoutis and female newborns of 272g (range 210-355g) in captivity. This can References probably be attributed to the diet and space under captive ANDERSON, R.R., SALAH, M.S., HARNESS, J.R. and SNEAD, conditions in this study. Moreover, whilst the average birth A.F., 1982. Mammary growth patterns in guinea pigs during weight of male newborn agoutis decreased as parturition puberty, pregnancy and lactation. Biology of Reproduction, vol. number increased from one to four, this was not significant 26, no. 4, pp. 620-627. PMid:6177352. http://dx.doi.org/10.1095/ and there was no difference between birth weight of female biolreprod26.4.620. young and parturition number. In the consulted literature, BAAS, E.J., POTKAY, S. and BACHER, J.D., 1976. The agouti we found no explanation for the obtained results. We can (Dasyprocta sp) in biomedical research and captivity. Laboratory suggest a higher intrauterine competition between males Animal Science, vol. 26, no. 5, pp. 788-796. PMid:185455. than females, which can be test in future research. BROWN-UDDENBERG, R., GARCIA, G.W., BAPTISTE, Q.S., The obtained results in this study suggests a low of COUNAND, T., ADOGWA, A.O. and SAMPSON, T., 2004. The dependence of newborn precocial agouti on maternal Agouti (Dasyprocta leporina, D. aguti) booklet and producers’ nutrition and may explain the large populations of wild manual. Saint Maurice: GWG Publications. 94 p. agouti, since newborn agouti may not necessarily need to suckle and possess the ability to feed themselves from birth CAMPOS, L.B., PEIXOTO, G.C.X., LIMA, G.L., CASTELO, T.S., SOUZA, A.L.P., OLIVEIRA, M.F. and SILVA, A.R., 2015. (Sikes and Ylonen, 1998), the generation interval may be Monitoramento do ciclo estral de cutias (Dasyprocta leporina decreased, resulting in growing populations of wild agouti Lichtenstein, 1823) através de citologia esfoliativa vaginal e in the Neotropics. Agouti population density ranges from ultrassonografia. Pesquisa Veterinária Brasileira, vol. 35, no. 2, pp. 8-84 individual agouti per km2 (Dubost et al., 2004; Jorge 188-192. http://dx.doi.org/10.1590/S0100-736X2015000200016.

Braz. J. Biol., 2018 , vol. 78, no. 3, pp. 540-547 545/547 545 Singh, M.D., Singh, S. and Garcia, G.W.

CUMMINS, I., PINEDO-VASQUEZ, M., BARNARD, A. and Amazonia. Biotropica, vol. 37, no. 2, pp. 317-321. http://dx.doi. NASI, R., 2015. Agouti on the wedding menu: bushmeat harvest, org/10.1111/j.1744-7429.2005.00041.x. consumption and trade in a post-frontier region of the Ecuadorian Amazon. Bogor: CIFOR. KIM, S.W., OSAKA, I., HURLEY, W.L. and EASTER, R.A., 1999. Mammary gland growth as influenced by litter size in DEEM, S.L., 2012. Disease risk analysis in wildlife health field lactating sows: impact on lysine requirement. Journal of Animal studies A2. In: R.E. MILLER, M. FOWLER, eds. Fowler’s zoo Science, vol. 77, no. 12, pp. 3316-3321. PMid:10641879. http:// and wild animal medicine. Amsterdam: Elsevier. chap. 1, pp. 2-7. dx.doi.org/10.2527/1999.77123316x. DE PETERS, E.J., & HOVEY, R.C., 2009. Methods for collecting KNIGHT, C.H. and WILDE, C.J., 1987. Mammary growth during milk from mice. Journal of Mammary Gland Biology and Neoplasia, lactation: implications for increasing milk yield. Journal of Dairy vol. 14, pp. 397-400. http://dx.doi.org/10.1007/s10911-009-9158-0. Science, vol. 70, no. 9, pp. 1991-2000. PMid:3668055. http:// dx.doi.org/10.3168/jds.S0022-0302(87)80241-2. DOLLINGER, P., BAUMGARTNER, R., ISENBUGEL, E., PAGAN, N., TENHU, H., and WEBER, F., (1999). Husbandry KNIGHT, C.H. and WILDE, C.J., 1993. Mammary cell changes and pathology of and lagomorphs in Swiss Zoos. Verh. during pregnancy and lactation. Livestock Production Science, vol. ber. Erkg. Zootiere, vol. 39, pp. 241-254. 35, no. 1, pp. 3-19. http://dx.doi.org/10.1016/0301-6226(93)90178-K. DUBOST, G., HENRY, O. and COMIZZOLI, P., 2004. Seasonality KORHONEN, H., 1992. Activated mammary number and litter of reproduction in the three largest terrestrial rodents of French size in the mink. Reproduction, Nutrition, Development, vol. Guiana forest. Mammalian Biology, vol. 70, no. 2, pp. 93-109. 32, no. 1, pp. 67-71. PMid:1575907. http://dx.doi.org/10.1051/ http://dx.doi.org/10.1016/j.mambio.2004.09.001. rnd:19920107. EMMONS, L. and REID, F. 2016 [viewed 29 November KORZ, V., 1991. Social-relations and individual coping reactions 2016]. Dasyprocta leporina (Linnaeus, 1758). The IUCN Red in a captive group of Central-American Agoutis (Dasyprocta- List of Threatened Species. e.T89497102A22197762. Available Punctata). Journal of Mammalogy, vol. 56, no. 4, pp. 207-218. from: http://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS. LE PENDU, Y., GUIMARAES, D.A. and LINHARES, Á., 2011. T89497102A22197762.en Estado da arte sobre a criação comercial da fauna silvestre brasileira. FARMER, C. 2013. Suckling effects in sows: importance for Revista Brasileira de Zootecnia, vol. 40, no. spe, pp. 52-59. mammary development and productivity. Animal: An International LOPES, J.B., CAVALCANTE, R.R., DE ALMEIDA, M.M., Journal of Animal Bioscience, vol. 7, no. 12, pp. 1964-1968. DE CARVALHO, M.M., DE MOURA, S.G., DANTAS, L. and http://dx.doi.org/10.1017/S1751731113001201. CONCEICAO, L.F., 2004. Performance of agouti (Dasyprocta FELDHAMMER, G.A., THOMPSON, B.C. and CHAPMAN, J.A., prymnolopha) bred in captivity according to sex and parturition in 2003. Wild mammals of North America: biology, management, Teresina, Piaui. Revista Brasileira de Zootecnia, vol. 33, no. 6, pp. and conservation. Baltimore: The John Hopkins University 2318-2322. http://dx.doi.org/10.1590/S1516-35982004000900018. Press. 1232 p. MERITT, D.A., 1983. Preliminary observations on reproduction in GILBERT, A.N., 1986. Mammary number and litter size in the Central American agouti, Dasyprocta punctata. Zoo Biology, vol. Rodentia: the “one-half rule”. Proceedings of the National 2, no. 2, pp. 127-131. http://dx.doi.org/10.1002/zoo.1430020205. Academy of Sciences of the United States of America, vol. 83, no. 13, pp. 4828-4830. PMid:16593720. http://dx.doi.org/10.1073/ NASI, R., TABER, A. and VAN VLIET, N., 2011. Empty forests, pnas.83.13.4828. empty stomachs? Bushmeat and livelihoods in the Congo and Amazon Basins. International Forestry Review, vol. 13, no. 3, GUIMARÃES, D.A., RAMOS, R.L., OHASHI, O.M., GARCIA, pp. 355-368. http://dx.doi.org/10.1505/146554811798293872. G.W. and VALE, W.G., 2011. Plasma concentration of progesterone and 17β-estradiol of black-rumped agouti (Dasyprocta prymnolopha) NOGUEIRA-FILHO, S.L.G. and NOGUEIRA, S.S.C., 2013. The during the estrous cycle. Revista de Biología Tropical, vol. 59, impact of management practices on female capybara reproductive no. 1, pp. 29-35. PMid:21513191. parameters in captivity. In: J.R. MOREIRA, K.M.P.M.B. FERRAZ, E.A. HERRERA, D.W. MACDONALD, eds. Capybara: biology, GUIMARÃES, D.A., ROSEMAR, R.L., GARCIA, G.W. use and conservation of an exceptional neotropical species. New and MITIO, O., 2009. The Stimulatory effect of male agouti York: Springer Science, pp. 275-282. (Dasyprocta prymnolopha) on the onset of female puberty. Acta Amazonica, vol. 39, no. 4, pp. 759-762. http://dx.doi.org/10.1590/ NOGUEIRA, S. and NOGUEIRA-FILHO, S.L.G., 2011. Wildlife S0044-59672009000400004. farming: an alternative to unsustainable hunting and deforestation in Neotropical forests? Biodiversity and Conservation, vol. 20, no. HAYSSEN, V., 1993. Empirical and theoretical constraints on 7, pp. 1385-1397. http://dx.doi.org/10.1007/s10531-011-0047-7. the evolution of lactation. Journal of Dairy Science, vol. 76, no. 10, pp. 3213-3233. PMid:8227642. http://dx.doi.org/10.3168/jds. OFTEDAL, O.T., 2000. Use of maternal reserves as a lactation S0022-0302(93)77659-6. strategy in large mammals. The Proceedings of the Nutrition Society, vol. 59, no. 1, pp. 99-106. PMid:10828179. http://dx.doi. HUGHES, E.S.R., 1950. The development of the mammary gland: org/10.1017/S0029665100000124. arris and gale lecture, delivered at the Royal College of Surgeons of England on 25th October, 1949. Annals of the Royal College OJASTI, J., 2000. Manejo de fauna silvestre neotropical. of Surgeons of England, vol. 6, no. 2, pp. 99-119. http://dx.doi. Washington, D.C.: Smithsonian Institution. 233 p. Biodiversity org/10.1530/jrf.0.0650521. PMid:19309885. Program, SI/MAB Series, 5. JORGE, M.S.P. and PERES, C.A., 2005. Population density and PAGELS, J.F., 2013. Mammalogy: Virginia master naturalist home range size of red-rumped agoutis (Dasyprocta leporina) course. In: Virginia Cooperative Extension, ed. Virginia tech. within and outside a natural Brazil Nut Stand in southeastern Virginia: VSU, pp. 3-14.

546 546/547 Braz. J. Biol., 2018 , vol. 78, no. 3, pp. 540-547 Mammary functionality in Dasyprocta leporina in captivity

PEREZ, E.M. and OJASTI, J., 1996. La utilization de la fauna SENGER, P.L., 2013. Pathways-to-pregnancy and parturition. silvestre en la America Tropical y Recomendaciones para su manejo 2nd ed. Pullman: Current Conceptions Inc. sustentable en las sabanas. Ecotropicos, vol. 9, no. 2, pp. 71-82. SIKES, R.S. and YLÖNEN, H., 1998. Considerations of optimal POND, C.M., 1977. The significance of lactation in the evolution litter size in mammals. Oikos, vol. 83, no. 3, pp. 452-465. http:// of mammals. Evolution; International Journal of Organic dx.doi.org/10.2307/3546673. Evolution, vol. 31, no. 1, pp. 177-199. PMid:28567732. http:// SINGH, M.D. and GARCIA, G.W., 2015. Perimortality in a dx.doi.org/10.1111/j.1558-5646.1977.tb00995.x. Captive Reared Agouti (Dasyprocta leporina). Wildlife Biology in Practice, vol. 11, no. 2, pp. 70-74. http://dx.doi.org/10.2461/ RACKAL, C.W., MOLLINEAU, W.M., MACFARLANE, R.A., wbp.2015.11.8. SINGH, M.D. and GARCIA, G.W., 2013. Wildlife farming in Trinidad. In: Proceedings of the 49th Caribbean Food Crops SINGH, M.D., ADOGWA, A.O., MOLLINEAU, W.M. and Society Meeting, June 30-July 6 2013, Trinidad and Tobago. 389 p. GARCIA, G.W., 2014. Gross and microscopic anatomy of the reproductive tract of the female agouti (Dasyprocta leporina): a ROBINSON, G.W., KARPF, A.B. and KRATOCHWIL, K., 1999. neotropical rodent with potential for food production. Tropical Regulation of mammary gland development by tissue interaction. Agriculture (St Augistine), vol. 91, no. 1, pp. 38-46. Journal of Mammary Gland Biology and Neoplasia, vol. 4, no. 1, pp. SMYTHE, N., 1978. The natural history of the Central American 9-19. PMid:10219903. http://dx.doi.org/10.1023/A:1018748418447. agouti (Dasyprocta punctata). Washington, D.C.: Smithsonian ROBINSON, J.G. and REDFORD, K.H., 1991. Sustainable Institution, pp. 1-52. Smithsonian Contributions to Zoology, no. harvest of neotropical forest mammals. In: J.G. ROBINSON and 257. http://dx.doi.org/10.5479/si.00810282.257. K.H. REDFORD, eds. Neotropical wildlife use and conservation. WEIR, B.J., 1971. Some observations on reproduction in the Chicago: Chicago University Press, pp. 415-429. female agouti, Dasyprocta aguti. Journal of Reproduction and Fertility, vol. 24, no. 2, pp. 203-211. PMid:5102535. http://dx.doi. ROBINSON, J.G. and REDFORD, K.H., 1994. Measuring the org/10.1530/jrf.0.0240203. sustainability of hunting in tropical forests. Oryx, vol. 28, no. 4, pp. 249-257. http://dx.doi.org/10.1017/S0030605300028647. WESTLIN, L.M. and GUSTAFSSON, T.O., 1983. Influence of sexual experience and social environment on fertility and incidence ROTH-KOLAR, H., 1957. Beitrage zum einem Aktionssystem of mating in young female bank voles (Clethrionomys glareolus). des Aguti. Zeitschrift für Tierpsychologie, vol. 14, no. 3, pp. Journal of Reproduction and Fertility, vol. 69, no. 1, pp. 173-177. 362-375. http://dx.doi.org/10.1111/j.1439-0310.1957.tb00543.x. PMid:6350570. http://dx.doi.org/10.1530/jrf.0.0690173.

Braz. J. Biol., 2018 , vol. 78, no. 3, pp. 540-547 547/547 547